impulsivity and semantic/emotional processing: an examination of the n400 wave

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Impulsivity and semantic/emotional processing: An examination of the N400 wave Vilfredo De Pascalis * , Brian Arwari, Laura D’Antuono, Immacolata Cacace Department of Psychology, University of Rome ‘‘La Sapienza, Via dei Marsi 78, 00185 Rome, Italy article info Article history: Accepted 11 October 2008 Available online 20 November 2008 Keywords: Impulsivity Language Event-related potentials N400 wave Semantic processes Affective processes abstract Objective: The study investigated (a) to what extent semantic/emotional processing modulates the N400 wave of the event-related potentials (ERPs) during reading, (b) the influence of impulsivity trait on neu- rocognitive systems underlying semantic/emotional processing related to the generation of the N400 wave. Methods: A canonical semantic sentence processing paradigm, known to selectively elicit the N400 wave was used. The ERPs were elicited to emotionally valenced (neutral, positive and negative) sentence final words that were either semantically congruent or semantically incongruent with the previous sentence context. Results: Congruent negatively valenced words produced longer reaction times (RTs) than congruent posi- tive and neutral words. Incongruent words elicited more pronounced N400 peak amplitudes than congru- ent ones, while, for the congruent trials, the N400 amplitude was greater for negative words as compared to positive and neutral words. High impulsive participants, compared to low impulsive ones, (a) made more errors and longer reaction times in identifying incongruent words, (b) displayed more pronounced N400 peak amplitudes over fronto-central midline scalp sites. Conclusions: This pattern of results indicated that the activity of fronto-central system may account for individual differences of impulsivity with high impulsive individuals showing more difficulty in integrat- ing incongruent final words into a sentence context. Significance: Results open up new perspectives for future investigations on language disorders character- ized by substantial impulsivity. Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. 1. Introduction Impulsivity has been defined as acting on the impetus of the moment without being aware of the potential risks involved (Eysenck et al., 1985; Patton et al., 1995), the tendency to act with- out much deliberation, which often results in fast and error-prone responding (Dickman, 1990; Daruna and Barnes, 1993), the tendency to act for immediate gratification, risky activities, novel sensations and easier routes of self-gratification (Mitchell, 1999). There are important individual differences in impulsivity (Depue and Collins, 1999; Gray and McNaughton, 2000; Revelle, 1997) and these are closely related to other personality constructs, such as extraversion, sensation seeking and psychopathy (Depue and Collins, 1999; Pickering and Gray, 2001; Revelle, 1997; Zuckerman and Kuhlman, 2000). Most findings suggest that impulsivity is multifactorial, although there is little agreement as to what these factors are (Evenden, 1999). Among others, it includes cognitive dimensions, such as decision time, response inhibition, timing, behavioral switching, motor impulsivity, premature responding and lack of persistence (Buss and Plomin, 1975; Evenden, 1999). Highly impulsive individuals consistently score low in vocabu- lary, reading comprehension, receptive and expressive language, sentence repetition and completion, and verbal intelligence and memory (Harmon-Jones et al., 1997; Lewis et al., 1980; Richman and Lindgren, 1981; Spellacy, 1977; Stanford et al., 1996). Impul- sivity coupled with deficits in verbal ability has been related to delinquent activities, poor school performance, and increased behavior problems (Maughan et al., 1996; Miller, 1988; Silva et al., 1987). Impulsivity, as well as incidence of physical and verbal aggression, is inversely correlated with reading accuracy, reading comprehension and verbal skills (Barratt et al., 1997; Harmon-Jones et al., 1997; Stanford et al., 1996). Personality traits like impulsivity or extraversion have been found associated with P300 wave of the ERP (see e.g., Daruna et al., 1985; De Pascalis, 2004; De Pascalis et al., 2004; De Pascalis and Speranza, 2000; Ortiz and Maojo, 1993; Russo et al., 2008; Polich and Martin, 1992; Pritchard, 1989; Stelmack et al., 1993), suggesting a reduced P300 amplitude in impulsive (and extra- verted) subjects. A negative relationship between impulsivity, reading levels and the amplitude of the P300 ERP component 1388-2457/$34.00 Ó 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.clinph.2008.10.008 * Corresponding author. Tel.: +39 06 76907199; fax: +30 0649917711. E-mail address: [email protected] (V. De Pascalis). Clinical Neurophysiology 120 (2009) 85–92 Contents lists available at ScienceDirect Clinical Neurophysiology journal homepage: www.elsevier.com/locate/clinph

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Page 1: Impulsivity and semantic/emotional processing: An examination of the N400 wave

Clinical Neurophysiology 120 (2009) 85–92

Contents lists available at ScienceDirect

Clinical Neurophysiology

journal homepage: www.elsevier .com/locate /c l inph

Impulsivity and semantic/emotional processing: An examination of the N400 wave

Vilfredo De Pascalis *, Brian Arwari, Laura D’Antuono, Immacolata CacaceDepartment of Psychology, University of Rome ‘‘La Sapienza”, Via dei Marsi 78, 00185 Rome, Italy

a r t i c l e i n f o

Article history:Accepted 11 October 2008Available online 20 November 2008

Keywords:ImpulsivityLanguageEvent-related potentialsN400 waveSemantic processesAffective processes

1388-2457/$34.00 � 2008 International Federation odoi:10.1016/j.clinph.2008.10.008

* Corresponding author. Tel.: +39 06 76907199; faxE-mail address: [email protected] (V. De Pasc

a b s t r a c t

Objective: The study investigated (a) to what extent semantic/emotional processing modulates the N400wave of the event-related potentials (ERPs) during reading, (b) the influence of impulsivity trait on neu-rocognitive systems underlying semantic/emotional processing related to the generation of the N400wave.Methods: A canonical semantic sentence processing paradigm, known to selectively elicit the N400 wavewas used. The ERPs were elicited to emotionally valenced (neutral, positive and negative) sentence finalwords that were either semantically congruent or semantically incongruent with the previous sentencecontext.Results: Congruent negatively valenced words produced longer reaction times (RTs) than congruent posi-tive and neutral words. Incongruent words elicited more pronounced N400 peak amplitudes than congru-ent ones, while, for the congruent trials, the N400 amplitude was greater for negative words as comparedto positive and neutral words. High impulsive participants, compared to low impulsive ones, (a) mademore errors and longer reaction times in identifying incongruent words, (b) displayed more pronouncedN400 peak amplitudes over fronto-central midline scalp sites.Conclusions: This pattern of results indicated that the activity of fronto-central system may account forindividual differences of impulsivity with high impulsive individuals showing more difficulty in integrat-ing incongruent final words into a sentence context.Significance: Results open up new perspectives for future investigations on language disorders character-ized by substantial impulsivity.� 2008 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights

reserved.

1. Introduction

Impulsivity has been defined as acting on the impetus of themoment without being aware of the potential risks involved(Eysenck et al., 1985; Patton et al., 1995), the tendency to act with-out much deliberation, which often results in fast and error-proneresponding (Dickman, 1990; Daruna and Barnes, 1993), thetendency to act for immediate gratification, risky activities, novelsensations and easier routes of self-gratification (Mitchell, 1999).There are important individual differences in impulsivity (Depueand Collins, 1999; Gray and McNaughton, 2000; Revelle, 1997)and these are closely related to other personality constructs, suchas extraversion, sensation seeking and psychopathy (Depue andCollins, 1999; Pickering and Gray, 2001; Revelle, 1997; Zuckermanand Kuhlman, 2000). Most findings suggest that impulsivity ismultifactorial, although there is little agreement as to what thesefactors are (Evenden, 1999). Among others, it includes cognitivedimensions, such as decision time, response inhibition, timing,

f Clinical Neurophysiology. Publish

: +30 0649917711.alis).

behavioral switching, motor impulsivity, premature respondingand lack of persistence (Buss and Plomin, 1975; Evenden, 1999).

Highly impulsive individuals consistently score low in vocabu-lary, reading comprehension, receptive and expressive language,sentence repetition and completion, and verbal intelligence andmemory (Harmon-Jones et al., 1997; Lewis et al., 1980; Richmanand Lindgren, 1981; Spellacy, 1977; Stanford et al., 1996). Impul-sivity coupled with deficits in verbal ability has been related todelinquent activities, poor school performance, and increasedbehavior problems (Maughan et al., 1996; Miller, 1988; Silvaet al., 1987). Impulsivity, as well as incidence of physical andverbal aggression, is inversely correlated with reading accuracy,reading comprehension and verbal skills (Barratt et al., 1997;Harmon-Jones et al., 1997; Stanford et al., 1996).

Personality traits like impulsivity or extraversion have beenfound associated with P300 wave of the ERP (see e.g., Darunaet al., 1985; De Pascalis, 2004; De Pascalis et al., 2004; De Pascalisand Speranza, 2000; Ortiz and Maojo, 1993; Russo et al., 2008;Polich and Martin, 1992; Pritchard, 1989; Stelmack et al., 1993),suggesting a reduced P300 amplitude in impulsive (and extra-verted) subjects. A negative relationship between impulsivity,reading levels and the amplitude of the P300 ERP component

ed by Elsevier Ireland Ltd. All rights reserved.

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86 V. De Pascalis et al. / Clinical Neurophysiology 120 (2009) 85–92

was also reported (e.g., Barratt et al., 1997). However, no enoughattention have been devoted in the literature in evaluating theinfluence of individual differences in impulsivity on ERP compo-nents during language processing. Among late ERP waves, theN400 have been suggested to reflect semantic processing. TheN400 is a broad negative ERP wave that peaks around 400 ms aftera semantically incongruous word in a meaningful sentence, such as‘The man liked his coffee with dog’ (Kutas and Federmeier, 2000). Itdoes not occur after syntactic incongruities or physical deviationssuch as changes in typescript (Kutas and Hillyard, 1980a,b). Theamplitude of the N400 is, in fact, an inverse function of the seman-tic congruence between the target word and the priming effectafforded by its prior context (Kutas and Hillyard, 1984), whetherthat context is a single word, sentence or discourse (van Berkumet al., 1999; Kutas, 1993; St. George et al., 1997).

It is known that emotionally unpleasant and pleasant stimulispontaneously arouse and capture the viewer’s attention and areprocessed in a facilitated manner. This stimulus driven reorienta-tion of attention helps to increase the chance with which poten-tially threatening or rewarding information can be perceived andevaluated (Lang et al., 1997; Bradley and Lang, 2000). A greatamount of evidence in support of this thesis comes from ERP stud-ies investigating temporal evolution of emotional picture process-ing. However, there is experimental evidence that verbal emotionalmaterial, due to its abstract description of emotional contents, isless perceptually engaging than other types of visual affectiveitems such as facial expressions or emotional pictures (Keil,2006; Kissler et al., 2006; Mogg and Bradley, 1998; Vanderploeget al., 1987; Codispoti et al., 2007). Consequently, emotional picto-rial material would be more capable of disrupting an ongoing cog-nitive task due to attentional capture than verbal emotionalstimuli. However, experimental evidence to support this is reallysparse and recent studies on cognitive interference by emotionalwords suggest that effects for processing of emotional words arequalitatively similar as effects found in pictures (or face) studies(see e.g., Keil, 2006; Ortigue et al., 2004; Karrétié et al., 2008; Kiss-ler et al., 2007; Herbert et al., 2008).

Among ERP studies investigating emotional word processing,the modulation of the N400 by emotional word content has hardlybeen investigated, although some studies have found amplitudevariations of N400 or N400-like waves to emotional words in nor-mal controls and in psychopaths (Kiehl et al., 1999; Williamsonet al., 1991). Usually, larger N400 amplitudes reflect a violationof semantic expectations and difficulties with context integration.However, Federmeier et al. (2001) provided experimental evidencethat mood can modulate N400 amplitude in sentence processing,as unexpected and distantly related spoken words elicit smallerN400 amplitudes in mildly positive mood, indicating facilitatedsemantic integration in positive mood. In a later study, Kieferand colleagues (Kiefer et al., 2007), investigating the effect of moodon cortical processing of pleasant and unpleasant adjectives, foundthat pleasant adjectives, in contrast to unpleasant adjectives, facil-itated semantic integration when subjects were in a positive moodas indexed by reduced N400 amplitudes. Very recently, Herbertand collaborators (Herbert et al., 2008) reported a facilitation pro-cessing selectively for pleasant adjectives that were associatedwith a reduced N400 and were also better remembered in an inci-dental memory test. Thus, there is experimental evidence suggest-ing that both a word’s emotional content and the participants’emotional state may affect the N400 ERP response.

On these bases, the purpose of the present study for the N400component was exploratory, because, as yet, very few experimen-tal studies have investigated the impact of emotional content onthis ERP wave. In particular, the present study attempted to exam-ine the simultaneous impact of word incongruency and emotionalcontent of a sentence final word on N400 amplitude and to deter-

mine whether: (a) semantically incongruent words elicited a morepronounced N400 wave as compared to congruent words; (b) pos-itively valenced words, in contrast to negative words, facilitatedsemantic integration as indexed by reduced N400 amplitudes.

Personality dimensional models have always emphasized rela-tionships between normal traits and personality disorders (seee.g., the five-factor model, Costa and Widiger, 2002). Within this tra-dition, the relationship with the Zuckerman–Kuhlman PersonalityQuestionnaire (ZKPQ; Zuckerman et al., 1993) is of particular inter-est because this provides an alternative five-factor structure that in-cludes five basic personality dimensions: Impulsive-unsocializedSensation Seeking (ImpSS), Neuroticism–Anxiety (N-Anx), Aggres-sivity–Hostility (Agg-Host), Activity (Act) and Sociability (Sy). Ingeneral, the relationships between Zuckerman’s model and person-ality disorders are still largely unknown. This personality model is ofparticular interest, however, providing as it does an alternative five-factor structure that includes, among others, a dimension of impul-sive sensation seeking that is of particular clinical significance.Impulsive sensation seeking is the most studied normal trait in rela-tion to personality disorders. For instance, Ball et al. (1994) foundthat Sensation Seeking correlated with antisocial personality andlife-time drug abuse and Thornquist and Zuckerman (1995) reportedsignificant correlations between ImpSS and Agg-Host with the totalscore of the Psychopathy Check List (Hare, 1991).

A number of ERP/language studies have been carried out for thepsychopathy, a germane personality dimension of impulsivity.Some studies found language abnormalities in psychopaths en-gaged in tasks requiring semantic processing (Hare, 1979; Hareand Forth, 1985; Hare and McPherson, 1984). In particular, Kiehland colleagues (1999) found that psychopathy is associated withlanguage abnormalities during semantic processing of abstractword stimuli. These authors, for non-psychopathic individuals, re-ported that concrete words elicited a greater negativity of theevent-related potential (ERP) in the 300–500 ms (i.e., N400) win-dow than did abstract words (Kiehl et al., 1999; Kounios andHolcomb, 1994; Paller et al., 1987). Psychopaths made more errorsthan did non-psychopaths when having to classify word stimuli asabstract during a concrete/abstract discrimination task and, inthese individuals, the normal electrocortical differentiation be-tween concrete and abstract words was lacking. These authors ar-gued that psychopaths may differ from others in the processresponsible for the generation of the N400 wave, i.e., to the processof integration of a word into ongoing cognitive context (Holcomb,1993; Kutas and Hillyard, 1980c, 1983, 1984). More recent findingsfailed to support this hypothesis (Kiehl et al., 2006b). However, in afurther study, Kiehl and collaborators (Kiehl et al., 2006a) foundthat processing of oddball targets elicited larger fronto-centralnegativities (N550), enlarged N2 and reduced P3 components inpsychopaths than in non-psychopaths. These findings were inter-preted as supporting the hypothesis that psychopathy may be re-lated to dysfunction of the paralimbic system—a system thatincludes parts of the temporal and frontal lobes.

Given the known link between psychopathy and impulsivity,and the known difficulty for impulsive individuals in reading andverbal processes (see e.g., Barratt et al., 1997; Harmon-Joneset al., 1997; Stanford et al., 1996), it is surprising that no attentionhas been devoted to examine how individual differences in impul-sivity may be reflected on N400 component of the ERPs duringsemantic/affective processing.

In line with previous findings, the aim of the present study was totest the hypothesis that high impulsive subjects, rated within a nor-mal range of impulsivity trait, should evidence more difficulty in theprocessing of semantic and affective verbal information. The use ofsentences ending with a semantically congruent or semanticallyincongruent neutral, negative and positive valenced word, in ourexperiment, permitted to evaluate whether previous N400 findings

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V. De Pascalis et al. / Clinical Neurophysiology 120 (2009) 85–92 87

observed for psychopaths could also be observed with emotionalstimuli in normal individuals differing in impulsivity levels. More-over, considering the link between impulsivity and sensation seek-ing (SS, Zuckerman, 1993, 2005), impulsivity-related differences inN400 amplitude will be investigated by controlling for individualdifferences in sensation seeking in order to highlight the pattern ofcovariation among these variables. Accordingly with the past litera-ture, we expected that high impulsive individuals would showpoorer behavioral performance and enhanced N400 waves forincongruent terminal words than would the low impulsive oneswith little or no differentiation between positive and negative emo-tional words.

2. Materials and methods

2.1. Participants

Participants were 56 right-handed women between the ages of19 and 36 years (M = 24.5, SD = 3.2). Hand preference was assessedwith the Italian version of the Edinburgh Handedness Inventory(Salmaso and Longoni, 1985).

Subjects were admitted to participate in the experiment only ifthey reported absence of drug abuse, use of medication (e.g., psy-choactive drugs, antihistamines) or medical conditions that mightinterfere with vigilance and task performance (e.g., high bloodpressure, diabetes mellitus, heart diseases, asthma, neurologicalor psychiatric disorders) and had 10/10 or corrected to 10/10 visionwith no history of neurological problems. In addition, participantswho were on their menstrual cycle or who had taken medicationthat might cause drowsiness or otherwise interfere with EEGrecordings, were rescheduled. In accordance with the ethicalnorms of the Italian Association of Psychology (AIP), all partici-pants gave informed consent prior to their inclusion in the study.Subjects performed their tasks during two sessions scheduledabout two weeks apart. During the first session all participantswere administered the Italian adaptation of the Zuckerman–Kuhlman Personality Questionnaire (ZKPQ; Zuckerman et al.,1993; De Pascalis and Russo, 2003). Seven subjects had gross EEGartifacts, one disattended the experimental session, thus 48woman volunteers were used for data analysis.

From the available qualified pool (N = 48 SS), two extreme-groupswere selected on the basis of impulsivity subscale of the ZKPQ. Thosepersons whose impulsivity score was respectively above the median(Md = 3.0) were defined as high impulsive subjects (Hi-Imp, n = 23,M = 5.3, SD = 1.3), while those persons whose impulsivity score wasbelow the median were defined as low impulsive subjects (Lo-Imp,n = 21; M = 0.9, SD = 0.9). It may be useful to emphasize that, at leastas far as we can tell, high- and low-impulsive subjects were psychiat-rically normal since impulsivity scores reported by the participantswere still within a normal range of impulsivity. The same can be saidfor sensation seeking scores (for normative scores see Zuckermanet al., 1993; De Pascalis and Russo, 2003).

In order to control the influence of gender factor on personal-ity measures, only women were invited to participate in theexperiment. Gender differences in ratings of impulsivity havebeen well documented in personality research, showing increasedimpulsivity scores in men (Miller, 1991; Nagoshi et al., 1991).Similarly, men significantly outscored females on sensation seek-ing and impulsive sensation seeking scores (Zuckerman et al.,1991, 1993; Aluja et al., 2003).

2.2. Stimuli

Two-hundred and seventy sentences (four to seven words inlength) were presented one word at a time on a computer monitor.

The number of syllables of sentence final words ranged from one tofour. Sentences ended with a word that was either semanticallycongruent (50% of trials) or semantically incongruent (50% of trials)with the previous sentence context. The order of sentence presen-tation was pseudo random. All words were presented in green let-ters (Arial font, 68 point) on a black background centered on a 15-in. computer monitor positioned about 100 cm from the partici-pant’s eyes. Word duration was of 350 ms. The second to last wordwas underlined to serve as a warning for the incoming last word(target). Inter-stimulus interval (ISI) between words was of1000 ms. The inter-trial interval (ITI) between two sentences wasof 2500 ms.

Sentences were grouped on the basis of emotional valence (po-sitive, negative, neutral) and congruence/incongruence into sixgroups, each formed of 45 sentences (positive/congruent, posi-tive/incongruent, negative/congruent, negative/incongruent, neu-tral/congruent, neutral/incongruent). Sentences were selectedfrom a sample of 600 rated by a group of 30 students on a 7-pointpleasant/unpleasant rating scale. Sentence final words rated asmore than 1.5 SDs above or below the mean pleasantness ratingswere defined as positive (e.g. ‘caress’) or negative (e.g., ‘dead’),respectively; neutral words (e.g., ‘bridge’) were those that fell lessthan.5 SDs from the mean. A subgroup of 50 subjects was requiredalso to rate the congruency/incongruency level on a 7-point likertscale. Words rated as more than 1.5 SDs above or below the meancongruency ratings were defined as ‘congruent’ or ‘incongruent’,respectively. The list of positive, negative and neutral sentence fi-nal words was defined in such a way that they were balanced forfrequency of use in Italian (De Mauro et al., 1993) [Frequency ofuse (per 490,000 words): M = 21.40, SD = 23.59, M = 19.22,SD = 38.72, and M = 31.67, SD = 41.77, respectively, for positive,negative and neutral words; all comparisons were not significant,all ts < 1]. Types of words were also balanced in number of sylla-bles, i.e., there were no significant differences on the number ofsyllables between emotional words [Number of syllables:M = 2.55, SD = .78, M = 2.50, SD = .73, and M = 2.47, SD = .57,respectively for positive, negative and neutral words; all compari-sons were not significant, all ts < 1].

2.3. Procedure

The subjects were seated in a comfortable reclining armchair,placed in a dimly lit, sound damped, and electrically shieldedbooth. Sentences were presented to the participants by using aone-by-one word reading paradigm. Subjects were invited to si-lently read each word and to press a right-handed button when-ever a sentence final word was congruent with the sentencecontext, and a left-handed button if the final word was incongruentwith sentence context. The hand used to make the response wascounterbalanced across participants. The experiment was dividedinto three 90 phrase blocks, each lasting about 10 min. After eachblock, subjects were allowed to rest for a few minutes. At theend of the EEG recordings, subject’s mood was measured usingthe Positive and Negative Affective Schedule (PANAS; Watsonet al., 1988). The PANAS, used widely in mood research, providesscores for two orthogonally related dimensions of mood states: po-sitive and negative. There are 10 adjectives covering positive affect(PANAS-PA), and 10 adjectives covering negative affect (PANAS-NA), and each affect is rated from 1 (‘very slightly or not at all’)to 5 (‘extremely’).

2.4. EEG recording and ERP measures

EEG and electro-ocular (EOG) were acquired continuously andsimultaneously with the performance measures by using a 40-channel NuAmps DC amplifier system (Neuroscan Inc.), set at a

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gain of 200, sampling rate of 500 Hz, and with signals band-lim-ited to 100 Hz. In addition, a 50 Hz notch filter was applied. Thesignals were amplified by NuAmp DC amplifiers (NeuroscanInc.). Data were recorded and stored on a computer running Neu-roscan Acquire 4.2 software. Electrode impedance was lower than3 kX. The horizontal EOG was monitored via a pair of tin elec-trodes placed 1 cm lateral to the outer canthus of each eye andthe vertical EOG was monitored via a separate bipolar montageplaced above and below the center of the left eye. EEG data wererecorded from 30 scalp sites (Fp1, Fp2, F7, F8, F3, F4, FT7, FT8, T3,T4, FC3, FC4, C3, C4, CP3, CP4, TP7, TP8, T5, T6, P3, P4, O1, O2, Fz,FCz, Cz, CPz, Pz, Oz) referenced to linked-ear electrodes by usingan electrocap (Blom and Anneveldt, 1982) with pure tin elec-trodes. The ground electrode was located 10 mm anterior to Fz.

The EEG was later reconstructed into discrete, single-trialepochs. For each sentence, an EEG epoch length of 1050-ms wasused with a 150-ms pre-stimulus baseline and a 900-ms periodfollowing the onset of the sentence final word. Epochs were re-jected from averaging if amplitude exceeded +75 lV, and eyeblinks were corrected for statistically in accordance with Grattonet al.’s procedure (Gratton et al., 1983). When the recording wassplit in two equal parts, the mean percentages of rejected trialswere ranging from 0.05 to 0.08. No participants had less than35 accepted trials in any condition. There were no significant dif-ferences between groups in the number of trials averaged in anycondition. All data average files were digitally filtered (15 Hz lowpass), and baseline corrected. An ERP response was obtained foreach of the six experimental conditions.

2.5. Performance, ERP measures and data analyses

The following performance measures were calculated: (1) FalseAlarm/Hit ratio (i.e., the ratio between the number of errors andthe number of correct target detections), (2) RT or the latency ofcorrect detections (i.e., the interval between the onset of the targetstimulus and the depressing of the response button), (3) Coefficientof Variation (CV) of the RT scores. These measures were submittedto a split-plot analysis of covariance (ANCOVA; SAS-8.02, glm pro-cedure) by considering impulsivity as the between groups factorand sensation seeking as the covariate. The experimental designwas the following: 2 Personality level (High, Low) � 3 Emotionalvalence (Positive, Negative, Neutral) � 2 Word congruency (Con-gruent, Incongruent).

Sentence final word stimuli elicited a centroparietal ERP neg-ativity with an approximate peak latency of 390 ± 18.0 ms. Wetermed this negative waveform as N400 wave since had similarshape to the known N400 wave typically observed in semanticword and sentence processing tasks (Kutas and Hillyard,1980c, 1983, 1984). For this ERP wave a mean amplitude mea-sure within a 300–420-ms time window from sentence finalword onset was provided. This time window was derived fromthe grand average waveform by centering on the peak of thiscomponent. For N400 amplitude scores, two separate ANCOVAswere performed. One ANCOVA was performed on midline elec-trodes location (Fz, FCz, Cz, CPz, Pz). A second ANCOVA was fo-cused on scalp quadrants (i.e., left-frontal: Fp1, F3, F7, FC3, FT7;right-frontal: Fp2, F4, F8, FC4, FT8; left-central: C3, T3, CP3;right-central: C4, T4, CP4; left-posterior: T5, TP7, P3, O1; right-posterior: T6, TP8, P4, O2). As for behavioral measures, bothanalyses had impulsivity as between factor and sensation seek-ing as covariate. The ANCOVA performed on the quadrant scoresincluded Personality level (High vs Low) as between-subjectsfactors and Hemisphere (Left vs Right), Site (Frontal, Central,Posterior), Word congruency (Congruous, Incongruous) andEmotional Valence (Positive, Negative, Neutral) as within-sub-jects factors. To prevent the risk of falsely significant results,

as may happen using repeated measures analysis if the spheric-ity assumption has been violated (Vasey and Thayer, 1987), theHuynh–Feldt epsilon correction of significance levels was ap-plied when necessary. Post hoc comparisons of the means wereperformed by using a t-test procedure with alpha = 0.05 (Kirk,1968, pp. 90–93).

The Pearson r coefficient and partial r of impulsivity and sensa-tion seeking measures with N400 amplitude were computed. Inaddition, N400 amplitude scalp measures were used as predictorsin separate stepwise regression analyses in order to assess theirpredictive power for impulsivity.

3. Results

3.1. Impulsivity, behavioral and self-reported data

High and low impulsive subjects did not differ in the falsealarm/hit ratio [F(1,41) = 1.69, p = 0.21; low impulsives, M = 0.21,SD = 0.15; high impulsives, M = 0.20, SD = 0.18]. Moreover, for con-gruent words, low impulsives had higher ratios than high impul-sives (M = 0.30, SD = .24, and M = 0.14, SD = 0.12, respectively),while an opposite trend was found for incongruent words betweenlow and high impulsivity groups (M = 0.15, SD = .17, and M = 0.21,SD = 0.28, respectively) [Impulsivity �Word congruency interac-tion, F(1, 41) = 6.08, p = 0.018].

Across all participants,negativevalenced words had longer RTthanpositive and neutral words [main effect of Emotional Valence,F(2,82) = 4.59, p = 0.0129; M = 1027.9 ms, SD = 128.0 vs M =965.9 ms, SD = 120.2, t = 5.93, p < .0001, and vs M = 962.6 ms,SD = 107.8, t = 6.49, p < .0001; for negative vs positive, and vs neutralwords, respectively]. Furthermore, congruent sentence negative finalwords produced a longer RT as compared to congruent positive andneutral words (M = 1071.1 ms, SD = 113.3 vs M = 939.0 ms,SD = 95.3, t = 8.40, p < .0001 and vs M = 909.9 ms, SD = 107.9;t = 9.54, p < .0001), while there were no significant differences amongincongruent negative, positive and neutral words (M = 992.3 ms,SD = 137.9 vs M = 1015.7 ms, SD = 115.8 t =�1.34, p > .05, and vsM = 1015.3 ms, SD = 118.7; t =�1.66, p > .05) [Emotional Valence� -Word congruency interaction, F(2,82) = 7.49, p = 0.002]. There wereno significant differences on RT scores between impulsivity groups[low impulsives, M = 971.8 ms, SD = 129.0; high impulsives,M = 986.8 ms, SD = 103.4; F(1,41) = 0.89, p = .352]. Nevertheless,low impulsives, for incongruent words, had shorter RTs thanhigh impulsives (M = 966.5 ms, SD = 83.4, and M = 1029.4 ms,SD = 149.9), while there were no RT differences between low and highimpulsivity groups for congruent words (M = 961.2 ms, SD = 97.4, andM = 964.1 ms, SD = 113.7) [Impulsivity �Word congruency interac-tion, F(1,41) = 4.47, p = 0.041].

The CV of the RT scores did not yield any significant effectinvolving Impulsivity, Emotional Valence or Word congruency.

High impulsives had higher PANAS-PA scores than low impul-sives (M = 2.9, SD = .6 vs M = 2.4, SD = .6; t = 2.22, p = .032), whilehigh and low impulsivity groups had the same PANAS-NA score(M = 1.3, SD = .38 vs M = 1.3, SD = .39; t < < 1).

3.2. Relationship between impulsivity, sensation seeking and positiveand negative affect measures

The ZKPQ measures of impulsivity and sensation seeking wereslightly, but significantly correlated (r = .316, p < .05). The positiveaffect, as measured with PANAS, was slightly correlated with sen-sation seeking (r = .295, p < .05), while the correlation between PA-NAS scores of negative did not reach the significance level (r = .12,p > .05).

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Fig. 2. Grand-average event-related potentials (ERPs) at frontal, central and parietalscalp quadrants for congruent (solid) and incongruent terminal words (dashed) ofsentences.

V. De Pascalis et al. / Clinical Neurophysiology 120 (2009) 85–92 89

There were no significant correlations between performancemeasures, i.e., False Alarm/Hit ratio, RT and CV of the RT scoresand impulsivity, with the exception of False Alarm/Hit ratio of po-sitive congruent words that was significantly correlated withimpulsivity (r = � 0.389, p < 0.006).

3.3. Impulsivity, N400 amplitude and semantic/emotional processing

There was a smaller overall N400 amplitude in low impulsivesas compared to high impulsives [main effect of impulsivity, mid-line, F(1,41) = 4.62, p = 0.037], although this difference was morepronounced over fronto-central and central sites [Impulsiv-ity � Site interaction, midline, F(2,82) = 4.90, p = 0.026; quadrants,F(2,82) = 5.62, p = 0.016] (see Fig. 1).

Across all participants, N400 was larger for incongruent thanfor congruent sentence endings [main effect of Word congruency,midline, F(1,41) = 57.2, p < 0.0001; M = �3.0, SD = 0.3 vs 0.03 lV,SD = 0.4; quadrants, F(1,41) = 49.07, p < 0.0001; M = �2.0, SE = 0.2vs 0.2 lV, SD = 0.2]. This effect was largest at central, centropari-etal and parietal midline sites [Word congruency � Site interac-tion, midline, F(4,164) = 3.72, p = 0.023; quadrants, F(2,82) = 3.73,p = 0.047]. The N400 for incongruent words was slightly largerover left hemisphere posterior sites and over the right hemispherefrontal and central sites than the analogous right and left hemi-sphere sites [Word congruency � Hemisphere � Site, quadrants,F(2,82) = 6.35, p = 0.0042]. This effect is displayed in Fig. 2.

Negative emotional words, as compared to positive and neutralwords, elicited a larger N400 wave over central and posterior sites[Emotional Valence � Site, quadrants, F(4,164) = 4.61, p = 0.006].Moreover, positive words elicited larger N400 waves in the rightas compared to the left hemisphere, while there were no hemi-spheric asymmetries for negative and neutral terminal words[Hemisphere � Emotional Valence, quadrants, F(2,82) = 4.75,p = 0.012]. This effect is shown in Fig. 3.

Considering that high impulsives scored significantly higher onPANAS-PA than low impulsives, two separate ANCOVAs were per-formed, respectively for midline and quadrant N400 amplitude

Fig. 1. Grand-average event-related potentials (ERPs) for high impulsives (black)and low impulsives (gray).

measures, by using median split PANAS-PA score as the betweengroups factors and Sensation Seeking as the covariate. No mainor interaction effects involving PANAS-PA were found to be signif-icant [PANAS-PA, midline, F(1,42) = 0.38, p = 0.538; quadrants,F(2,82) = 0.70, p = 0.408; 0.4 < F < 2 for all interactions involvingPANAS-PA factor]. These lacking differences indicated that

Fig. 3. Grand-average event-related potentials (ERPs) at frontal, central and parietalscalp quadrants for negative (dashed), neutral (gray) and positive (solid) emotionalterminal words of sentences.

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differential N400 results found between impulsivity groups werenot due to differences in positive affect.

3.4. Predictors of impulsivity

Correlation coefficients were calculated between midline N400amplitude measures and the impulsivity scores. There were sig-nificant negative correlations between impulsivity and N400amplitude elicited by neutral, positive and negative words overmidline frontal and fronto-central sites. However, the highest cor-relation was found for neutral incongruent words at fronto-cen-tral site. These correlations are reported in Table 1. As it can beclearly seen in Table 1, the relationship between impulsivityand N400 amplitude was not affected after controlling for Sensa-tion Seeking (compare the first and second column in Table 1).

In order to highlight which of the significantly correlatedbehavioral and N400 amplitude measures was the best predictorof impulsivity, a stepwise regression analysis was conductedusing False Alarm/Hit ratio, and N400 amplitude over Fz, andFCz sites for neutral, positive and negative words as predictors.This procedure retained the N400 amplitude at FCz scalp siteand False Alarm/Hit ratio for Neutral incongruent words as thebest predictors of impulsivity scores (beta = �0.31, F = 12.62,p = 0.0009; beta = �2.60, F = 4.61, p = 0.037, respectively forN400 amplitude at FCz and False Alarm/Hit ratio). The regressionmodel was statistically significant [F(2,47) = 11,46; p < 0.0001]with N400 measure accounting for the 27.0% of the total variance[F = 16.99, p = 0.0002] and False Alarm/Hit ratio accounting forthe 6.8% of the total variance, with no other variables enteringin the equation. The adjusted R-square for the total equation

Table 1Correlation between N400 amplitude at midline and impulsivity (Imp) and partial rafter controlling for sensation seeking (SS).

Imp Controlling for SS

Congruent wordsFz-Neu �0.417 �0.401FCz-Neu �0.370 �0.360Cz-Neu �0.248 �0.244CPz-Neu �0.229 �0.215Pz-Neu �0.181 �0.165Fz-Pos �0.284 �0.264FCz-Pos �0.304 �0.283Cz-Pos �0.192 �0.169CPz-Pos �0.219 �0.198Pz-Pos �0.180 �0.161Fz-Neg �0.268 �0.222FCz-Neg �0.300 �0.241Cz-Neg �0.201 �0.131CPz-Neg �0.135 �0.067Pz-Neg �0.082 �0.011

Incongruent wordsFz-Neu �0.317 �0.351FCz-Neu �0.519 �0.544Cz-Neu �0.275 �0.295CPz-Neu �0.269 �0.281Pz-Neu �0.190 �0.200Fz-Pos �0.287 �0.292FCz-Pos �0.310 �0.309Cz-Pos �0.211 �0.226CPz-Pos �0.213 �0.229Pz-Pos �0.121 �0.139Fz-Neg �0.290 �0.274FCz-Neg �0.253 �0.254Cz-Neg �0.076 �0.096CPz-Neg �0.044 �0.061Pz-Neg �0.012 �0.037

Note: Bold, p < .01; Italic, p < .05.

was of 0.31. The scatterplot for the most significant correlationbetween impulsivity and N400 measure is reported in Fig. 4.

4. Conclusion

The present study was designed to examine (a) the simulta-neous impact of word incongruency and emotional content onbehavioral performance and N400 wave of the ERPs as elicited bya sentence final word, and (b) the relationship between impulsivityand N400 amplitude during emotional word processing.

In terms of semantic processing, as expected, it was found thatsemantically sentence incongruent final words elicited a more pro-nounced N400 wave as compared to congruent ones. This finding isin line with the classic evidence that N400 amplitude is, in fact, aninverse function of the semantic congruence between the targetword and the priming effect afforded by its prior context (Kutasand Hillyard, 1984; van Berkum et al., 1999; Kutas, 1993; St.George et al., 1997). In terms of emotional word processing, for po-sitive valenced words compared to negative words, shorter RTs andsmaller N400 amplitudes were evidenced. This finding was seen asindicating facilitated semantic integration for positive valencedwords, a finding that is in line with previous reports by Federmeieret al. (2001), wherein spoken words elicited smaller N400 ampli-tudes in mildly positive mood, and by Kiefer et al. (2007) and Her-bert et al. (2008) reporting facilitated semantic integration, i.e.,reduced N400 amplitudes to pleasant adjectives reading comparedto unpleasant adjectives reading. Furthermore, in terms of behav-ioral performance, this study has provided experimental evidencethat congruency interacted with emotional valence of sentence fi-nal word given that congruent positive words had shorter RTs thancongruent negative words, while there were no significant differ-ences for incongruent words.

High impulsive subjects, compared to low impulsive ones, madelonger RTs and more errors when categorizing incongruent words,while there were no RT differences between impulsivity groups forcongruent words. This finding is in line with previous reports sug-gesting that impulsives have more difficulty in processing complexinformation (Harmon-Jones et al., 1997; Schweizer, 2002).

In terms of N400 amplitude, high impulsive participants, ascompared to low impulsive ones, had more pronounced peaks ofthis ERP component over fronto-central scalp regions for eithercongruent or incongruent sentence final words. This finding gener-ally supported the prediction that normal impulsive individualswould not show significant ERP differentiation between congruentand incongruent words and between positive and negative words.These observations resembled those previously reported betweeninmate psychopaths and non-psychopaths for oddball target detec-tion (Kiehl et al., 2006a), emotional polarity discrimination (Kiehl

Fig. 4. Scatterplot illustrating the relationship between impulsivity and N400amplitude at fronto-central (FCz) scalp site for emotionally neutral incongruentterminal words of sentences.

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et al., 1999), and emotional lexical decision task (Williamson et al.,1991) wherein ERPs of psychopaths did not differentiate word typeand were found associated with aberrant larger negativities in the300–600 ms time window. There are at least two possible interpre-tations of the lack of significant ERP word type effects for theimpulsive participants. First, it may be that impulsives simply donot differentiate word stimuli in a matter similar to that foundwith non-impulsives. Second, impulsives may differ from othersin the time course and degree of activation necessary to differenti-ate between word stimuli. This latter interpretation is strength-ened by the presence of behavioral differences for incongruentwords between impulsivity groups. It may also be the case thatimpulsives were using an alternative strategy to perform the tasks,although the exact nature of this strategy is not known.

Interestingly, stepwise correlational analyses indicated thatfronto-central N400 amplitude and false alarm/hit ratio for neutralincongruent words, were the best predictors of impulsivity by,respectively, accounting for 27% and 6.8% of the total variance. Thisfinding also parallels the significant correlation between psychop-athy and N400 amplitude reported by Kiehl et al. (1999). However,to the best of our knowledge no study analyzed the N400/Impul-sivity relationship controlling for individual differences in sensa-tion seeking. On this issue, a relevant result of the present studyis that N400/Impulsivity relationship is not affected when control-ling for sensation seeking, the latter being positively correlatedwith impulsivity.

It is important to note that there are some limitations to thisstudy that should be addressed in future research. First, our find-ings are restricted to a sample of only women and cannot be ex-tended to the general population, especially because there isexperimental evidence for increased impulsivity in men (Miller,1991; Nagoshi et al., 1991). This procedure if on the one handhas produced more homogeneous behavioral and N400 data scoreswith a relatively small sample size, from the other hand has leavedout possible main or interactional effects of gender with impulsiv-ity factor. Second, direct measures of language fluency and readingability were not assessed in the present study. Thus, we cannot to-tally exclude that these factors may have influenced the observeddifferences between impulsivity groups even if all the participantswere undergraduate psychology students.

In summary, although impulsivity is thought to play a crucialrole in emotional processes (Gray and McNaughton, 2000), thepresent findings have evidenced that this personality trait is alsoassociated with differences in semantic aspects of languageprocessing.

In this respect, this research suggests that impulsive individualsare associated with increased difficulty in the processing of lan-guage. This may place impulsives at a clear disadvantage in teach-ing programs and may indicate that these individuals need ofalternative forms of teaching.

In conclusion, our behavioral and N400 findings suggest thatimpulsivity is associated with abnormalities in the scalp-recorded potentials associated with the integration process ofinformation conveyed by a final word into a sentence contextand that these abnormalities appear to be localized to the fron-to-central cortical region and surrounding cortex. However, itshould be outlined that this interpretation is speculative and fur-ther studies using a greater number of participants includinggender factor are needed before any robust conclusions can becarried out.

Acknowledgments

We wish to thank Mr. Sante Moretti, and Mr. Pietro Fermani(Department of Psychology University of Rome ‘‘La Sapienza”),for technical support.

This study was supported by a biennal grant from the Faculty ofPsychology-1, and AST, University of Rome ‘‘La Sapienza” to A.A.(Years: 2006-07 to A.A. prots. C26F06MW7H and C26F07472B).

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